The Ubiquitin C-Terminal Hydrolase L1 (UCH-L1) C terminus plays a key role in protein stability, but its farnesylation is not required for membrane association in primary neurons

Journal of Biological Chemistry

Volumn 289, Issue 52, 2014, Pages 36140-36149

  Bishop, Paul ^a   Rubin, Philip ^a   Thomson, Andrew R ^a   Rocca, Dan ^a   Henley, Jeremy M ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CULTURE; CELL DEATH; CLONE CELLS; ENZYME ACTIVITY; HYDROLASES; NEURODEGENERATIVE DISEASES; NEURONS; PROTEINS;

DEUBIQUITINATING ENZYMES; INTRACELLULAR DISTRIBUTION; MEMBRANE ASSOCIATION; NEURODEGENERATION; NEUROFIBRILLARY TANGLES; PARKINSON DISEASE; PROTEIN SOLUBILITY; PROTEIN STABILITY;

MEMBRANES;

UBIQUITIN THIOLESTERASE; UBIQUITIN THIOLESTERASE L1; UNCLASSIFIED DRUG; UCH-L1 PROTEIN, RAT;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; BINDING AFFINITY; BRAIN CELL CULTURE; CARBOXY TERMINAL SEQUENCE; CELL SEPARATION; CLONAL CELL LINE; CONTROLLED STUDY; EMBRYO; ENZYME BINDING; ENZYME ISOLATION; ENZYME LOCALIZATION; FARNESYLATION; HUMAN; HUMAN CELL; MEMBRANE BINDING; NERVE CELL MEMBRANE; NERVE CELL NECROSIS; NONHUMAN; PROTEIN AGGREGATION; PROTEIN MISFOLDING; PROTEIN SECONDARY STRUCTURE; PROTEIN STABILITY; PROTEIN STRUCTURE; PROTEIN UNFOLDING; RAT; STRUCTURE ACTIVITY RELATION; STRUCTURE ANALYSIS; ANIMAL; APOPTOSIS; CELL MEMBRANE; CHLOROCEBUS AETHIOPS; COS 1 CELL LINE; HEK293 CELL LINE; METABOLISM; NERVE CELL; PRIMARY CELL CULTURE; PROTEIN PRENYLATION; PROTEIN TERTIARY STRUCTURE; PROTEIN TRANSPORT; UBIQUITINATION;

ANIMALS; APOPTOSIS; CELL MEMBRANE; CERCOPITHECUS AETHIOPS; COS CELLS; HEK293 CELLS; HUMANS; NEURONS; PRIMARY CELL CULTURE; PROTEIN PRENYLATION; PROTEIN STABILITY; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; RATS; UBIQUITIN THIOLESTERASE; UBIQUITINATION;

EID: 84919936064     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.557124     Document Type: Article

References (38)

1. Hershko, A., and Ciechanover, A. (1998) The ubiquitin system. Annu. Rev. Biochem. 67, 425-479
2. Mabb, A. M., and Ehlers, M. D. (2010) Ubiquitination in postsynaptic function and plasticity. Annu. Rev. Cell Dev. Biol. 26, 179-210
3. Ross, C. A., and Poirier, M. A. (2004) Protein aggregation and neurodegenerative disease. Nat. Med. 10, S10-S17
4. Blokhuis, A. M., Groen, E. J., Koppers, M., van den Berg, L. H., and Pasterkamp, R. J. (2013) Protein aggregation in amyotrophic lateral sclerosis. Acta Neuropathol. 125, 777-794
5. Wilkinson, K. D., Lee, K. M., Deshpande, S., Duerksen-Hughes, P., Boss, J. M., and Pohl, J. (1989) The neuron-specific protein PGP 9.5 is a ubiquitin carboxyl-terminal hydrolase. Science 246, 670-673
6. Osaka, H., Wang, Y. L., Takada, K., Takizawa, S., Setsuie, R., Li, H., Sato, Y., Nishikawa, K., Sun, Y. J., Sakurai, M., Harada, T., Hara, Y., Kimura, I., Chiba, S., Namikawa, K., Kiyama, H., Noda, M., Aoki, S., and Wada, K. (2003) Ubiquitin carboxy-terminal hydrolase L1 binds to and stabilizes monoubiquitin in neuron. Hum. Mol. Genet. 12, 1945-1958
7. Kurihara, L. J., Semenova, E., Levorse, J. M., and Tilghman, S. M. (2000) Expression and functional analysis of Uch-L3 during mouse development. Mol. Cell. Biol. 20, 2498-2504
8. Liu, Y., Fallon, L., Lashuel, H. A., Liu, Z., and Lansbury, P. T., Jr. (2002) The UCH-L1 gene encodes two opposing enzymatic activities that affect α-synuclein degradation and Parkinson's disease susceptibility. Cell 111, 209-218
9. Liu, Z., Meray, R. K., Grammatopoulos, T. N., Fredenburg, R. A., Cookson, M. R., Liu, Y., Logan, T., and Lansbury, P. T., Jr. (2009) Membrane-associated farnesylated UCH-L1 promotes α-synuclein neurotoxicity and is a therapeutic target for Parkinson's disease. Proc. Natl. Acad. Sci. U.S.A. 106, 4635-4640
10. Nagamine, S., Kabuta, T., Furuta, A., Yamamoto, K., Takahashi, A., and Wada, K. (2010) Deficiency of ubiquitin carboxy-terminal hydrolase-L1 (UCH-L1) leads to vulnerability to lipid peroxidation. Neurochem. Int. 57, 102-110
11. Chen, J., Huang, R. Y., and Turko, I. V. (2013) Mass spectrometry assessment of ubiquitin carboxyl-terminal hydrolase L1 partitioning between soluble and particulate brain homogenate fractions. Anal. Chem. 85, 6011-6017
12. Spillantini, M. G., Crowther, R. A., Jakes, R., Hasegawa, M., and Goedert, M. (1998) α-Synuclein in filamentous inclusions of Lewy bodies from Parkinson's disease and dementia with Lewy bodies. Proc. Natl. Acad. Sci. U.S.A. 95, 6469-6473
13. Cartier, A. E., Ubhi, K., Spencer, B., Vazquez-Roque, R. A., Kosberg, K. A., Fourgeaud, L., Kanayson, P., Patrick, C., Rockenstein, E., Patrick, G. N., and Masliah, E. (2012) Differential effects of UCHL1 modulation on α-synuclein in PD-like models of α-synucleinopathy. PLoS ONE 7, e34713
14. Choi, J., Levey, A. I., Weintraub, S. T., Rees, H. D., Gearing, M., Chin, L. S., and Li, L. (2004) Oxidative modifications and down-regulation of ubiquitin carboxyl-terminal hydrolase L1 associated with idiopathic Parkinson's and Alzheimer's diseases. J. Biol. Chem. 279, 13256-13264
15. Koharudin, L. M., Liu, H., Di Maio, R., Kodali, R. B., Graham, S. H., and Gronenborn, A. M. (2010) Cyclopentenone prostaglandin-induced unfolding and aggregation of the Parkinson disease-associated UCH-L1. Proc. Natl. Acad. Sci. U.S.A. 107, 6835-6840
16. Perestenko, P. V., and Henley, J. M. (2003) Characterization of the intracellular transport of GluR1 and GluR2 α-amino-3-hydroxy-5-methyl-4- isoxazole propionic acid receptor subunits in hippocampal neurons. J. Biol. Chem. 278, 43525-43532
17. Kantamneni, S., Correa, S. A., Hodgkinson, G. K., Meyer, G., Vinh, N. N., Henley, J. M., and Nishimune, A. (2007) GISP: a novel brain-specific protein that promotes surface expression and function of GABA(B) receptors. J. Neurochem. 100, 1003-1017
18. Navarro-Lérida, I., Sánchez-Perales, S., Calvo, M., Rentero, C., Zheng, Y., Enrich, C., and Del Pozo, M. A. (2012) A palmitoylation switch mechanism regulates Rac1 function and membrane organization. EMBO J. 31, 534-551
19. Boyartchuk, V. L., Ashby, M. N., and Rine, J. (1997) Modulation of Ras and a-factor function by carboxyl-terminal proteolysis. Science 275, 1796-1800
20. Apolloni, A., Prior, I. A., Lindsay, M., Parton, R. G., and Hancock, J. F. (2000) H-ras but not K-ras traffics to the plasma membrane through the exocytic pathway. Mol. Cell. Biol. 20, 2475-2487
21. Zhang, F. L., and Casey, P. J. (1996) Protein prenylation: molecular mechanisms and functional consequences. Annu. Rev. Biochem. 65, 241-269
22. Meray, R. K., and Lansbury, P. T., Jr. (2007) Reversible monoubiquitination regulates the Parkinson disease-associated ubiquitin hydrolase UCHL1. J. Biol. Chem. 282, 10567-10575
23. Leroy, E., Boyer, R., Auburger, G., Leube, B., Ulm, G., Mezey, E., Harta, G., Brownstein, M. J., Jonnalagada, S., Chernova, T., Dehejia, A., Lavedan, C., Gasser, T., Steinbach, P. J., Wilkinson, K. D., and Polymeropoulos, M. H. (1998) The ubiquitin pathway in Parkinson's disease. Nature 395, 451-452
24. Kabuta, T., Setsuie, R., Mitsui, T., Kinugawa, A., Sakurai, M., Aoki, S., Uchida, K., and Wada, K. (2008) Aberrant molecular properties shared by familial Parkinson's disease-associated mutant UCH-L1 and carbonylmodified UCH-L1. Hum. Mol. Genet. 17, 1482-1496
25. Sułkowska, J. I., Rawdon, E. J., Millett, K. C., Onuchic, J. N., and Stasiak, A. (2012) Conservation of complex knotting and slipknotting patterns in proteins. Proc. Natl. Acad. Sci. U.S.A. 109, E1715-E1723
26. Fang, Y., Fu, D., and Shen, X. Z. (2010) The potential role of ubiquitin c-terminal hydrolases in oncogenesis. Biochim. Biophys. Acta 1806, 1-6
27. Das, C., Hoang, Q. Q., Kreinbring, C. A., Luchansky, S. J., Meray, R. K., Ray, S. S., Lansbury, P. T., Ringe, D., and Petsko, G. A. (2006) Structural basis for conformational plasticity of the Parkinson's disease-associated ubiquitin hydrolase UCH-L1. Proc. Natl. Acad. Sci. U.S.A. 103, 4675-4680
28. Lowe, J., McDermott, H., Landon, M., Mayer, R. J., and Wilkinson, K. D. (1990) Ubiquitin carboxyl-terminal hydrolase (PGP 9.5) is selectively present in ubiquitinated inclusion bodies characteristic of human neurodegenerative diseases. J. Pathol. 161, 153-160
29. Kaplan, A., and Stockwell, B. R. (2012) Therapeutic approaches to preventing cell death in Huntington disease. Prog. Neurobiol. 99, 262-280
30. Sommer, D. B., and Stacy, M. A. (2008) What's in the pipeline for the treatment of Parkinson's disease? Expert Rev. Neurother. 8, 1829-1839
31. Andersson, F. I., Werrell, E. F., McMorran, L., Crone, W. J., Das, C., Hsu, S. T., and Jackson, S. E. (2011) The effect of Parkinson's-disease-associated mutations on the deubiquitinating enzyme UCH-L1. J. Mol. Biol. 407, 261-272
32. Chiti, F., and Dobson, C. M. (2006) Protein misfolding, functional amyloid, and human disease. Annu. Rev. Biochem. 75, 333-366
33. Bolognesi, B., Kumita, J. R., Barros, T. P., Esbjorner, E. K., Luheshi, L. M., Crowther, D. C., Wilson, M. R., Dobson, C. M., Favrin, G., and Yerbury, J. J. (2010) ANS binding reveals common features of cytotoxic amyloid species. ACS Chem. Biol. 5, 735-740
34. Last, N. B., and Miranker, A. D. (2013) Common mechanism unites membrane poration by amyloid and antimicrobial peptides. Proc. Natl. Acad. Sci. U.S.A. 110, 6382-6387
35. Evangelisti, E., Cecchi, C., Cascella, R., Sgromo, C., Becatti, M., Dobson, C. M., Chiti, F., and Stefani, M. (2012) Membrane lipid composition and its physicochemical properties define cell vulnerability to aberrant protein oligomers. J. Cell Sci. 125, 2416-2427
36. Gidalevitz, T., Ben-Zvi, A., Ho, K. H., Brignull, H. R., and Morimoto, R. I. (2006) Progressive disruption of cellular protein folding in models of polyglutamine diseases. Science 311, 1471-1474
37. Olzscha, H., Schermann, S. M., Woerner, A. C., Pinkert, S., Hecht, M. H., Tartaglia, G. G., Vendruscolo, M., Hayer-Hartl, M., Hartl, F. U., and Vabulas, R. M. (2011) Amyloid-like aggregates sequester numerous metastable proteins with essential cellular functions. Cell 144, 67-78
38. Wang, Y., Geer, L. Y., Chappey, C., Kans, J. A., and Bryant, S. H. (2000) Cn3D: sequence and structure views for Entrez. Trends Biochem. Sci. 25, 300-302